517
Journal of Parkinson’s Disease 4 (2014) 517–521 DOI 10.3233/JPD-140380 IOS Press
Research Report
Caregiver Burden in Patients with Parkinson Disease Undergoing Deep Brain Stimulation: An Exploratory Analysis Michael J. Soileaua , Carol Persadb,c , Jennifer Taylorc , Parag G. Patilc,d,e and Kelvin L. Chouc,d,e,∗ a Department
of Neurology, University of Texas Medical School, Houston, Houston, TX, USA of Psychiatry, Division of Neuropsychology, University of Michigan, Ann Arbor, MI, USA c Surgical Therapies Improving Movement Program, University of Michigan, Ann Arbor, MI, USA d Department of Neurosurgery, University of Michigan, Ann Arbor, MI, USA e Department of Neurology, University of Michigan, Ann Arbor, MI, USA b Department
Abstract. Background: Little is known about caregiver burden in Parkinson disease (PD) patients undergoing brain stimulation (DBS) surgery. Objective: The aim of this exploratory analysis was to evaluate whether caregiver burden improves after bilateral subthalamic nucleus (STN) DBS for PD patients and identify baseline factors associated with caregiver burden. Methods: We analyzed the motor, cognitive and behavioral data of 12 PD patients (9 men/3 women) who underwent bilateral STN DBS and whose caregivers completed the Caregiver Burden Inventory (CBI) both before and approximately 6 months after bilateral STN DBS. Results: Total CBI score did not change from baseline (17.8 ± 10.7) to the 6 month evaluation (18.7 ± 13.1), despite a 29% improvement in the MDS-UPDRS motor score (baseline 40.3 ± 12.1 compared to 28.7 ± 8.4 at 6 months, p = 0.01). Change in total CBI score did not correlate with change in MDS-UPDRS Parts I–IV or MoCA from baseline to 6 months. In post-hoc analyses looking at baseline characteristics that may correlate with caregiver burden, only the disinhibition subscore on the Frontal Systems Behavioral Scale correlated positively with the baseline total CBI score (ρ = 0.763, p = 0.004). Conclusion: Caregiver burden for PD patients (as measured by the CBI) does not change 6 months after bilateral STN DBS, despite significant improvement in motor function. Only baseline behavioral problems, specifically disinhibition, correlated with higher baseline caregiver burden. Clinicians may need to better counsel patients on expectations for caregiver burden after DBS. Keywords: Parkinson disease, caregiver burden, deep brain stimulation, subthalamic nucleus
INTRODUCTION Caring for a patient with a complex neurodegenerative disease such as Parkinson disease (PD) may negatively impact the mental, social and physical health of the caregiver [1, 2]. Caregiver burden is ∗ Correspondence to: Kelvin L. Chou, MD, University of Michigan Medical School, 2301 Commonwealth Blvd., Ann Arbor, MI 48105-2945, USA. Tel.: +1 734 936 3087; Fax: +1 734 232 1170; E-mail: [email protected].
defined as the caregiver’s perception of stress caused from taking care of the patient’s physical, emotional, psychological, and socio-economical consequences of the disease. Specific aspects of caregiver burden that cause significant stress in these individuals include the level of care required for activities of daily living, the perception of the caregiver’s ability to control the disease, financial burden, inadequate education of PD, and the perceived support system in place to assist in dealing with PD [3]. Other studies find that caregiver
ISSN 1877-7171/14/$27.50 © 2014 – IOS Press and the authors. All rights reserved
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M.J. Soileau et al. / Caregiver Burden in STN DBS
burden is significantly associated with a patient’s advancing age, later stage of illness, and those having longer duration of caring [1, 2, 4, 5]. As such, caregiver burden is an important consideration for clinicians to keep in mind when they are treating PD patients. Bilateral deep brain stimulation (DBS) of the subthalamic nucleus (STN) is a well-established therapy for PD and long-term effectiveness on the main motor symptoms of PD, motor fluctuations, and dyskinesias have been well documented [6]. Little is known about caregiver burden in PD patients undergoing DBS. Oyama et. al. performed a cross-sectional retrospective study of 275 PD patients who had undergone DBS surgery and found that caregiver strain did not differ between the DBS group and a matched nonDBS group, suggesting that caregiver strain does not worsen with DBS [7]. However, caregiver strain was only examined post-operatively. Because there was no pre-surgical comparison, it remains unclear if caregiver burden improves with DBS surgery. We performed a retrospective study to evaluate whether caregiver burden improves after PD patients undergo bilateral STN DBS surgery given that motor function improves significantly after DBS surgery. A secondary aim was to explore whether cognitive or behavioral factors were associated with caregiver burden in patients undergoing DBS surgery. PATIENTS AND METHODS Patients We analyzed the clinical data of PD patients who have undergone bilateral STN DBS surgery at our institution. Patient selection criteria for DBS at our institution have been previously described [8]. Briefly, PD patients qualified for DBS if they had motor fluctuations despite optimal medication management or a disabling tremor despite treatment with high doses of levodopa. None had dementia based on formal neuropsychological evaluation at baseline. Patients with major untreated depression or psychosis were also excluded from surgery. The study was conducted in accordance with the policies of the Institutional Review Board of the University of Michigan for studies involving human subjects. All patients provided written informed consent. DBS Surgery Patients underwent DBS surgery in two stages, which has been previously described in detail [8]. Dur-
ing Stage 1, quadripolar DBS electrodes (Model 3389, Medtronic, Minneapolis, MN) were implanted into the subthalamic nuclei (STN) bilaterally. Intraoperatively, microelectrode recording and macroelectrode stimulation testing were used to optimize placement. Stage 2, occurring approximately 4 weeks after Stage 1, consisted of placement of the implantable pulse generator connected to the implanted lead. Initial programming of the stimulator took place approximately 2–3 weeks after stage 2. Evaluation and assessments All DBS patients undergo clinical assessments prior to surgery and approximately 6 months after initial programming. The Caregiver Burden Inventory (CBI) was introduced in May 2010 as part of this evaluation process, where both patients and their main caregiver participate in the assessment. The CBI is a 24-item questionnaire measuring caregiver burden across 5 separate domains including time dependency, development, physical health, social relationships, and emotional health [9]. The inventory is scored using a 5-point Likert scale ranging from 0 (not at all disruptive) to 4 (very disruptive.) A total score >36 indicates a risk of burn out whereas a score near or slightly above 24 indicates a need to seek some form of respite care. In addition to the CBI, each patient completed the following assessments before and after surgery: Movement Disorders Society revision of the Unified PD Rating Scale (MDS-UPDRS) and Montreal Cognitive Assessment (MoCA). The following behavioral assessments were completed at baseline: Modified Marin Apathy Evaluation Scale, State-Trait Anxiety, Geriatric depression Score (GDS), and the Frontal Systems Behavioral scale (FrSBe). Statistical analysis The change in performance on the CBI and other assessments from baseline to the 6 month postoperative evaluation was compared using the Wilcoxon signed rank test because of the small sample size. Comparison of CBI scores between men and women were performed using the Mann-Whitney test. Spearman rank correlation coefficient was used to evaluate correlations between the CBI and other baseline variables. Statistical analysis was performed with IBM SPSS Statistics v. 20.0 for Windows (Armonk, NY, IBM Corp). The significance level was set at p = 0.05, but Bonferroni correction was applied to adjust for multiple comparisons.
M.J. Soileau et al. / Caregiver Burden in STN DBS
RESULTS We analyzed 12 patients (3 F/9 M) who prospectively completed the CBI before and approximately 6 months after initial programming (mean 232.4 ± 20.0 days after DBS surgery). See Table 1 for the baseline characteristics of the cohort. All were at Hoehn and Yahr Stage 2 at the time of surgery. There was no change in the total CBI or its subscores with DBS. The MDS-UPDRS Part III score improved significantly by 11.6 points (29%) at 6 months ON stimulation/OFF medication compared to the baseline OFF medication score. The MDS-UPDRS Part IV improved by 59% at 6 months, but Parts I and II and the MoCA did not significantly improve. Because CBI did not change, we conducted a post-hoc analysis looking at whether any baseline demographics were associated with an increased baseline CBI score. There was no difference in baseline CBI scores between men (18.2 ± 11.1) and women (16.3 ± 11.8, p = 0.727). Baseline CBI score did not correlate with age or disease duration. We then looked at whether motor, cognitive or behavioral scores were correlated with increased CBI at baseline. Only the patient’s FrSBe disinhibition subscore correlated with the baseline CBI score, even after Bonferroni correction (ρ = 0.763, p = 0.004, see Fig. 1). The CBI did not correlate with the FrSBe apathy subscore, executive function subscore or total score, Parts I-IV of the MDS-UPDRS, MoCA, MAS, or the GDS. Finally, we evaluated relations between the change in total CBI score from baseline to 6 months and change in other assessments. Change in total CBI score did not correlate with change in MDS-UPDRS Parts I-IV or MoCA from baseline to 6 months.
DISCUSSION The aim of this exploratory study was to see if caregiver burden, as assessed with the CBI, improved with STN DBS. In our small cohort, neither the total CBI score nor its subscores changed at the 6 month evaluation. This is consistent with the study by Oyama et al., who administered the multidimensional caregiver strain index and PDQ-39 to 275 PD patients after DBS surgery, and compared their results to a matched group of PD patients that did not undergo DBS [7]. They were concerned that caregiver strain might worsen after DBS because of increased time demands and financial burden, but instead, they found that caregiver strain was not different between the DBS and non-DBS groups.
519
Their conclusions were limited though because they did not have a pre-surgical comparison. We expand on their results by examining caregiver burden both before and after DBS and hypothesized that caregiver burden would improve as motor symptoms improve. In our study, both the motor examination and motor complications subscores of the MDS-UPDRS improved significantly at 6 months after DBS surgery, while the CBI scores remained unchanged, suggesting the caregiver burden does not improve with STN DBS surgery despite motor improvement. A possible explanation for our results is that caregiver and social networks surrounding PD patients are developed gradually over time, so it may not be realistic to expect these networks to change so rapidly. Another possibility is that much of the first six months are an adjustment period, spent finding the balance between stimulation and medications. The amount of motor improvement may not have been reached until just before the 6 month assessment, so caregivers may not have perceived a benefit yet. It may be necessary to assess caregiver burden several months after motor function is optimized in order to see an improvement. However, we found no correlation between baseline CBI, motor aspects of daily living, motor severity or motor fluctuations (as assessed by MDS-UPDRS Parts II–IV) in our study, suggesting that caregiver burden in PD patients undergoing DBS is not associated with motor function. Caregiver burden in PD has been consistently associated with the Hoehn and Yahr stage, a measure of disease severity [1, 2, 5, 10], but has been variably associated with the UPDRS motor score [10, 11]. Our cohort was uniform in terms of disease severity with all subjects at Hoehn and Yahr stage 2. Finally, the average caregiver burden score in our cohort was low, going from 17.8 ± 10.7 at baseline to 18.7 ± 13.1 at the 6 month evaluation. A CBI score less than 24 indicates that caregivers are not as likely to need respite. Only 3 caregivers gave scores greater than 24, and only one caregiver had a CBI score greater than 36, which indicates a high risk of burnout. It may be that the CBI scores in our cohort were so low that there was a floor effect and scores could not possibly improve further. We did find a significant correlation between one behavioral variable, the FrSBe disinhibition subscore as rated by the subject and baseline caregiver burden. The FrSBe scale is a validated measure to help characterize behavior disturbances related to frontal system dysfunction. It consists of a 46 item questionnaire with each question falling into a 3 part assessment of apathy, disinhibition, and executive function [12]. Nei-
520
M.J. Soileau et al. / Caregiver Burden in STN DBS Table 1 Characteristics of PD subjects (n = 12) before and after bilateral STN DBS
Age (years) Gender Disease Duration (years) Levodopa Equivalent Dose (mg) MDS-UPDRS – Part I MDS-UPDRS – Part II MDS-UPDRS – Part III (off medications) MDS-UPDRS – Part IV MoCA Marin Apathy Scale (caregiver) Geriatric Depression Scale FrSBe Total FrSBe Apathy FrSBe Disinhibition FrSBe Executive Function CBI Total Score CBI – Time Dependency Score CBI – Development Score CBI – Physical Health Score CBI – Social Relationships Score CBI – Emotional Health Score
Baseline
6 months post-DBS
66.5 (7.2) 9 M/3 F 10.6 (4.7) 1360.0 (621.8) 13.7 (5.5) 17.9 (8.2)
– – – 805.8 (435.2) 12.4 (6.8) 14.3 (7.0)
P-value – – – 0.003∗ 0.25 0.39
40.3 (12.1) 9.0 (4.7) 25.0 (3.3) 8.3 (7.0) 2.8 (3.3) 59.8 (18.9) 59.6 (14.1) 56.3 (18.2) 57.8 (18.1) 17.8 (10.7) 6.1 (3.1) 4.3 (4.3) 2.8 (2.4) 2.7 (2.5) 1.8 (3.2)
28.7 (8.4) 3.7 (2.9) 25.7 (3.4) – – – – – – 18.7 (13.1) 7.2 (4.7) 4.0 (2.8) 3.2 (2.9) 2.3 (2.6) 2.1 (4.3)
0.003∗ 0.006∗ 0.07
0.44 0.40 0.72 0.67 0.62 0.85
∗ p < 0.05.
All values expressed as mean (SD) unless otherwise indicated. MDS-UPDRS = Movement Disorders Society revision of the Unified PD Rating Scale. MoCA = Montreal Cognitive Assessment. FrSBe = Frontal Systems Behavior Scale. CBI = Caregiver Burden Inventory.
Fig. 1. Correlation between baseline Caregiver Burden Inventory Total score and the Disinhibition subscore of the Frontal Systems Behavioral Scale.
ther apathy, disinhibition or executive function would be expected to improve with STN DBS, so it is not surprising that caregiver burden did not improve at 6 months. One study of 16 subjects who completed the FrSBe before and an average of 40 months after
bilateral STN DBS surgery found that all FrSBe subscale scores worsened significantly [13]. It is unclear if this was due to DBS or progression of PD. We will be collecting post-operative FrSBe assessments in this cohort to see if FrSBe scores worsen and if they
M.J. Soileau et al. / Caregiver Burden in STN DBS
are associated with increased caregiver burden after DBS. There was no correlation between CBI and global cognitive function as assessed by the MoCA in our cohort. Cognition may impact caregiver burden in PD, but only PD dementia has been found to increase caregiver burden [11]. One must keep in mind that part of the inclusion criteria for consideration for DBS surgery includes absence of dementia. Key limitations of the current study include the small number of patients and the short follow-up. Additionally, the CBI has not been validated in PD patients and it is unclear if it is responsive to treatment effects or change in this population. It will be important to gather data further out from surgery, to see if caregiver burden changes with time. Nevertheless, we found that behavioral issues, specifically disinhibition, correlate significantly with baseline caregiver burden in PD patients undergoing DBS surgery. Baseline caregiver burden (as assessed with the CBI) did not change 6 months after DBS despite significantly improved motor function. These findings are important to consider when counseling caregivers and patients about post-surgery expectations regarding caregiver burden. ACKNOWLEDGMENTS We would like to thank Susan Grube and Karen S. Cummings for helping us with data collection. Dr. Soileau has no disclosures. Dr. Persad receives support from NIH grants NS015655-26A1 and AG031951, University of Michigan M-CASTL RFP2010-04. She is also a co-investigator in a clinical trial supported by University Health Network/Michael J Fox Foundation for Parkinson’s Research. Dr. Taylor receives research support from the National Center for Research Resources (NCRR) (grant number UL1RR024986). Dr. Patil receives research support from the National Institutes of Health, the American Parkinson’s Disease Association, the Coulter Foundation, the Foundation for Physical Therapy, the Parkinson’s Disease Foundation, Michigan Institute for Clinical and Health Research, and the University of Michigan Department of Neurosurgery. Dr. Chou receives research support from the NIH (NS44504-08, 5R44NS070438) and the Michael J. Fox Foundation, participates as a site-PI in clinical trials sponsored by the Huntington Study Group (2CARE), receives royalties from UpToDate, receives royalties from Demos Health for his book Deep Brain Stimulation; A New
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Life for People with Parkinson’s, Dystonia, and Essential Tremor, and serves as a consultant for Medtronic and Accordant. CONFLICT OF INTEREST Financial disclosure related to research covered in this article: The authors report no conflicts of interest related to the research covered in this article. REFERENCES [1]
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Martinez-Martin P, Forjaz MJ, Frades-Payo B, Rusinol AB, Fernandez-Garcia JM, Benito-Leon J, Arillo VC, Barbera MA, Sordo MP, & Catalan MJ (2007) Caregiver burden in Parkinson’s disease. Mov Disord, 22, 924-931; quiz, 1060. Schrag A, Hovris A, Morley D, Quinn N, & Jahanshahi M (2006) Caregiver-burden in parkinson’s disease is closely associated with psychiatric symptoms, falls, and disability. Parkinsonism Relat Disord, 12, 35-41. Roland KP, Jenkins ME, & Johnson AM (2010) An exploration of the burden experienced by spousal caregivers of individuals with Parkinson’s disease. Mov Disord, 25, 189193. Razali R, Ahmad F, Rahman FN, Midin M, & Sidi H (2011) Burden of care among caregivers of patients with Parkinson disease: A cross-sectional study. Clin Neurol Neurosurg, 113, 639-643. Martinez-Martin P, Arroyo S, Rojo-Abuin JM, RodriguezBlazquez C, Frades B, & de Pedro Cuesta J (2008) Burden, perceived health status, and mood among caregivers of Parkinson’s disease patients. Mov Disord, 23, 1673-1680. Benabid AL, Chabardes S, Mitrofanis J, & Pollak P (2009) Deep brain stimulation of the subthalamic nucleus for the treatment of Parkinson’s disease. Lancet Neurol, 8, 67-81. Oyama G, Okun MS, Schmidt P, Troster AI, Nutt J, Go CL, Foote KD, Malaty IA, & Investigators N-Q (2014) Deep Brain Stimulation May Improve Quality of Life in People With Parkinson’s Disease Without Affecting Caregiver Burden. Neuromodulation, 17, 126-132. Patil PG, Conrad EC, Aldridge JW, Chenevert TL, & Chou KL (2012) The anatomical and electrophysiological subthalamic nucleus visualized by 3-T magnetic resonance imaging. Neurosurgery 71, 1089-1095; discussion, 1095. Novak M, & Guest C (1989) Application of a multidimensional caregiver burden inventory. Gerontologist, 29, 798-803. D’Amelio M, Terruso V, Palmeri B, Di Benedetto N, Famoso G, Cottone P, Aridon P, Ragonese P, & Savettieri G (2009) Predictors of caregiver burden in partners of patients with Parkinson’s disease. Neurol Sci, 30, 171-174. Leroi I, McDonald K, Pantula H, & Harbishettar V (2012) Cognitive impairment in Parkinson disease: Impact on quality of life, disability, and caregiver burden. J Geriatr Psychiatry Neurol, 25, 208-214. Stout JC, Ready RE, Grace J, Malloy PF, & Paulsen JS (2003) Factor analysis of the frontal systems behavior scale (FrSBe). Assessment, 10, 79-85. Denheyer M, Kiss ZH, & Haffenden AM (2009) Behavioral effects of subthalamic deep brain stimulation in Parkinson’s disease. Neuropsychologia, 47, 3203-3209.
Journal of Parkinson’s Disease 4 (2014) 517–521 DOI 10.3233/JPD-140380 IOS Press
Research Report
Caregiver Burden in Patients with Parkinson Disease Undergoing Deep Brain Stimulation: An Exploratory Analysis Michael J. Soileaua , Carol Persadb,c , Jennifer Taylorc , Parag G. Patilc,d,e and Kelvin L. Chouc,d,e,∗ a Department
of Neurology, University of Texas Medical School, Houston, Houston, TX, USA of Psychiatry, Division of Neuropsychology, University of Michigan, Ann Arbor, MI, USA c Surgical Therapies Improving Movement Program, University of Michigan, Ann Arbor, MI, USA d Department of Neurosurgery, University of Michigan, Ann Arbor, MI, USA e Department of Neurology, University of Michigan, Ann Arbor, MI, USA b Department
Abstract. Background: Little is known about caregiver burden in Parkinson disease (PD) patients undergoing brain stimulation (DBS) surgery. Objective: The aim of this exploratory analysis was to evaluate whether caregiver burden improves after bilateral subthalamic nucleus (STN) DBS for PD patients and identify baseline factors associated with caregiver burden. Methods: We analyzed the motor, cognitive and behavioral data of 12 PD patients (9 men/3 women) who underwent bilateral STN DBS and whose caregivers completed the Caregiver Burden Inventory (CBI) both before and approximately 6 months after bilateral STN DBS. Results: Total CBI score did not change from baseline (17.8 ± 10.7) to the 6 month evaluation (18.7 ± 13.1), despite a 29% improvement in the MDS-UPDRS motor score (baseline 40.3 ± 12.1 compared to 28.7 ± 8.4 at 6 months, p = 0.01). Change in total CBI score did not correlate with change in MDS-UPDRS Parts I–IV or MoCA from baseline to 6 months. In post-hoc analyses looking at baseline characteristics that may correlate with caregiver burden, only the disinhibition subscore on the Frontal Systems Behavioral Scale correlated positively with the baseline total CBI score (ρ = 0.763, p = 0.004). Conclusion: Caregiver burden for PD patients (as measured by the CBI) does not change 6 months after bilateral STN DBS, despite significant improvement in motor function. Only baseline behavioral problems, specifically disinhibition, correlated with higher baseline caregiver burden. Clinicians may need to better counsel patients on expectations for caregiver burden after DBS. Keywords: Parkinson disease, caregiver burden, deep brain stimulation, subthalamic nucleus
INTRODUCTION Caring for a patient with a complex neurodegenerative disease such as Parkinson disease (PD) may negatively impact the mental, social and physical health of the caregiver [1, 2]. Caregiver burden is ∗ Correspondence to: Kelvin L. Chou, MD, University of Michigan Medical School, 2301 Commonwealth Blvd., Ann Arbor, MI 48105-2945, USA. Tel.: +1 734 936 3087; Fax: +1 734 232 1170; E-mail: [email protected].
defined as the caregiver’s perception of stress caused from taking care of the patient’s physical, emotional, psychological, and socio-economical consequences of the disease. Specific aspects of caregiver burden that cause significant stress in these individuals include the level of care required for activities of daily living, the perception of the caregiver’s ability to control the disease, financial burden, inadequate education of PD, and the perceived support system in place to assist in dealing with PD [3]. Other studies find that caregiver
ISSN 1877-7171/14/$27.50 © 2014 – IOS Press and the authors. All rights reserved
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M.J. Soileau et al. / Caregiver Burden in STN DBS
burden is significantly associated with a patient’s advancing age, later stage of illness, and those having longer duration of caring [1, 2, 4, 5]. As such, caregiver burden is an important consideration for clinicians to keep in mind when they are treating PD patients. Bilateral deep brain stimulation (DBS) of the subthalamic nucleus (STN) is a well-established therapy for PD and long-term effectiveness on the main motor symptoms of PD, motor fluctuations, and dyskinesias have been well documented [6]. Little is known about caregiver burden in PD patients undergoing DBS. Oyama et. al. performed a cross-sectional retrospective study of 275 PD patients who had undergone DBS surgery and found that caregiver strain did not differ between the DBS group and a matched nonDBS group, suggesting that caregiver strain does not worsen with DBS [7]. However, caregiver strain was only examined post-operatively. Because there was no pre-surgical comparison, it remains unclear if caregiver burden improves with DBS surgery. We performed a retrospective study to evaluate whether caregiver burden improves after PD patients undergo bilateral STN DBS surgery given that motor function improves significantly after DBS surgery. A secondary aim was to explore whether cognitive or behavioral factors were associated with caregiver burden in patients undergoing DBS surgery. PATIENTS AND METHODS Patients We analyzed the clinical data of PD patients who have undergone bilateral STN DBS surgery at our institution. Patient selection criteria for DBS at our institution have been previously described [8]. Briefly, PD patients qualified for DBS if they had motor fluctuations despite optimal medication management or a disabling tremor despite treatment with high doses of levodopa. None had dementia based on formal neuropsychological evaluation at baseline. Patients with major untreated depression or psychosis were also excluded from surgery. The study was conducted in accordance with the policies of the Institutional Review Board of the University of Michigan for studies involving human subjects. All patients provided written informed consent. DBS Surgery Patients underwent DBS surgery in two stages, which has been previously described in detail [8]. Dur-
ing Stage 1, quadripolar DBS electrodes (Model 3389, Medtronic, Minneapolis, MN) were implanted into the subthalamic nuclei (STN) bilaterally. Intraoperatively, microelectrode recording and macroelectrode stimulation testing were used to optimize placement. Stage 2, occurring approximately 4 weeks after Stage 1, consisted of placement of the implantable pulse generator connected to the implanted lead. Initial programming of the stimulator took place approximately 2–3 weeks after stage 2. Evaluation and assessments All DBS patients undergo clinical assessments prior to surgery and approximately 6 months after initial programming. The Caregiver Burden Inventory (CBI) was introduced in May 2010 as part of this evaluation process, where both patients and their main caregiver participate in the assessment. The CBI is a 24-item questionnaire measuring caregiver burden across 5 separate domains including time dependency, development, physical health, social relationships, and emotional health [9]. The inventory is scored using a 5-point Likert scale ranging from 0 (not at all disruptive) to 4 (very disruptive.) A total score >36 indicates a risk of burn out whereas a score near or slightly above 24 indicates a need to seek some form of respite care. In addition to the CBI, each patient completed the following assessments before and after surgery: Movement Disorders Society revision of the Unified PD Rating Scale (MDS-UPDRS) and Montreal Cognitive Assessment (MoCA). The following behavioral assessments were completed at baseline: Modified Marin Apathy Evaluation Scale, State-Trait Anxiety, Geriatric depression Score (GDS), and the Frontal Systems Behavioral scale (FrSBe). Statistical analysis The change in performance on the CBI and other assessments from baseline to the 6 month postoperative evaluation was compared using the Wilcoxon signed rank test because of the small sample size. Comparison of CBI scores between men and women were performed using the Mann-Whitney test. Spearman rank correlation coefficient was used to evaluate correlations between the CBI and other baseline variables. Statistical analysis was performed with IBM SPSS Statistics v. 20.0 for Windows (Armonk, NY, IBM Corp). The significance level was set at p = 0.05, but Bonferroni correction was applied to adjust for multiple comparisons.
M.J. Soileau et al. / Caregiver Burden in STN DBS
RESULTS We analyzed 12 patients (3 F/9 M) who prospectively completed the CBI before and approximately 6 months after initial programming (mean 232.4 ± 20.0 days after DBS surgery). See Table 1 for the baseline characteristics of the cohort. All were at Hoehn and Yahr Stage 2 at the time of surgery. There was no change in the total CBI or its subscores with DBS. The MDS-UPDRS Part III score improved significantly by 11.6 points (29%) at 6 months ON stimulation/OFF medication compared to the baseline OFF medication score. The MDS-UPDRS Part IV improved by 59% at 6 months, but Parts I and II and the MoCA did not significantly improve. Because CBI did not change, we conducted a post-hoc analysis looking at whether any baseline demographics were associated with an increased baseline CBI score. There was no difference in baseline CBI scores between men (18.2 ± 11.1) and women (16.3 ± 11.8, p = 0.727). Baseline CBI score did not correlate with age or disease duration. We then looked at whether motor, cognitive or behavioral scores were correlated with increased CBI at baseline. Only the patient’s FrSBe disinhibition subscore correlated with the baseline CBI score, even after Bonferroni correction (ρ = 0.763, p = 0.004, see Fig. 1). The CBI did not correlate with the FrSBe apathy subscore, executive function subscore or total score, Parts I-IV of the MDS-UPDRS, MoCA, MAS, or the GDS. Finally, we evaluated relations between the change in total CBI score from baseline to 6 months and change in other assessments. Change in total CBI score did not correlate with change in MDS-UPDRS Parts I-IV or MoCA from baseline to 6 months.
DISCUSSION The aim of this exploratory study was to see if caregiver burden, as assessed with the CBI, improved with STN DBS. In our small cohort, neither the total CBI score nor its subscores changed at the 6 month evaluation. This is consistent with the study by Oyama et al., who administered the multidimensional caregiver strain index and PDQ-39 to 275 PD patients after DBS surgery, and compared their results to a matched group of PD patients that did not undergo DBS [7]. They were concerned that caregiver strain might worsen after DBS because of increased time demands and financial burden, but instead, they found that caregiver strain was not different between the DBS and non-DBS groups.
519
Their conclusions were limited though because they did not have a pre-surgical comparison. We expand on their results by examining caregiver burden both before and after DBS and hypothesized that caregiver burden would improve as motor symptoms improve. In our study, both the motor examination and motor complications subscores of the MDS-UPDRS improved significantly at 6 months after DBS surgery, while the CBI scores remained unchanged, suggesting the caregiver burden does not improve with STN DBS surgery despite motor improvement. A possible explanation for our results is that caregiver and social networks surrounding PD patients are developed gradually over time, so it may not be realistic to expect these networks to change so rapidly. Another possibility is that much of the first six months are an adjustment period, spent finding the balance between stimulation and medications. The amount of motor improvement may not have been reached until just before the 6 month assessment, so caregivers may not have perceived a benefit yet. It may be necessary to assess caregiver burden several months after motor function is optimized in order to see an improvement. However, we found no correlation between baseline CBI, motor aspects of daily living, motor severity or motor fluctuations (as assessed by MDS-UPDRS Parts II–IV) in our study, suggesting that caregiver burden in PD patients undergoing DBS is not associated with motor function. Caregiver burden in PD has been consistently associated with the Hoehn and Yahr stage, a measure of disease severity [1, 2, 5, 10], but has been variably associated with the UPDRS motor score [10, 11]. Our cohort was uniform in terms of disease severity with all subjects at Hoehn and Yahr stage 2. Finally, the average caregiver burden score in our cohort was low, going from 17.8 ± 10.7 at baseline to 18.7 ± 13.1 at the 6 month evaluation. A CBI score less than 24 indicates that caregivers are not as likely to need respite. Only 3 caregivers gave scores greater than 24, and only one caregiver had a CBI score greater than 36, which indicates a high risk of burnout. It may be that the CBI scores in our cohort were so low that there was a floor effect and scores could not possibly improve further. We did find a significant correlation between one behavioral variable, the FrSBe disinhibition subscore as rated by the subject and baseline caregiver burden. The FrSBe scale is a validated measure to help characterize behavior disturbances related to frontal system dysfunction. It consists of a 46 item questionnaire with each question falling into a 3 part assessment of apathy, disinhibition, and executive function [12]. Nei-
520
M.J. Soileau et al. / Caregiver Burden in STN DBS Table 1 Characteristics of PD subjects (n = 12) before and after bilateral STN DBS
Age (years) Gender Disease Duration (years) Levodopa Equivalent Dose (mg) MDS-UPDRS – Part I MDS-UPDRS – Part II MDS-UPDRS – Part III (off medications) MDS-UPDRS – Part IV MoCA Marin Apathy Scale (caregiver) Geriatric Depression Scale FrSBe Total FrSBe Apathy FrSBe Disinhibition FrSBe Executive Function CBI Total Score CBI – Time Dependency Score CBI – Development Score CBI – Physical Health Score CBI – Social Relationships Score CBI – Emotional Health Score
Baseline
6 months post-DBS
66.5 (7.2) 9 M/3 F 10.6 (4.7) 1360.0 (621.8) 13.7 (5.5) 17.9 (8.2)
– – – 805.8 (435.2) 12.4 (6.8) 14.3 (7.0)
P-value – – – 0.003∗ 0.25 0.39
40.3 (12.1) 9.0 (4.7) 25.0 (3.3) 8.3 (7.0) 2.8 (3.3) 59.8 (18.9) 59.6 (14.1) 56.3 (18.2) 57.8 (18.1) 17.8 (10.7) 6.1 (3.1) 4.3 (4.3) 2.8 (2.4) 2.7 (2.5) 1.8 (3.2)
28.7 (8.4) 3.7 (2.9) 25.7 (3.4) – – – – – – 18.7 (13.1) 7.2 (4.7) 4.0 (2.8) 3.2 (2.9) 2.3 (2.6) 2.1 (4.3)
0.003∗ 0.006∗ 0.07
0.44 0.40 0.72 0.67 0.62 0.85
∗ p < 0.05.
All values expressed as mean (SD) unless otherwise indicated. MDS-UPDRS = Movement Disorders Society revision of the Unified PD Rating Scale. MoCA = Montreal Cognitive Assessment. FrSBe = Frontal Systems Behavior Scale. CBI = Caregiver Burden Inventory.
Fig. 1. Correlation between baseline Caregiver Burden Inventory Total score and the Disinhibition subscore of the Frontal Systems Behavioral Scale.
ther apathy, disinhibition or executive function would be expected to improve with STN DBS, so it is not surprising that caregiver burden did not improve at 6 months. One study of 16 subjects who completed the FrSBe before and an average of 40 months after
bilateral STN DBS surgery found that all FrSBe subscale scores worsened significantly [13]. It is unclear if this was due to DBS or progression of PD. We will be collecting post-operative FrSBe assessments in this cohort to see if FrSBe scores worsen and if they
M.J. Soileau et al. / Caregiver Burden in STN DBS
are associated with increased caregiver burden after DBS. There was no correlation between CBI and global cognitive function as assessed by the MoCA in our cohort. Cognition may impact caregiver burden in PD, but only PD dementia has been found to increase caregiver burden [11]. One must keep in mind that part of the inclusion criteria for consideration for DBS surgery includes absence of dementia. Key limitations of the current study include the small number of patients and the short follow-up. Additionally, the CBI has not been validated in PD patients and it is unclear if it is responsive to treatment effects or change in this population. It will be important to gather data further out from surgery, to see if caregiver burden changes with time. Nevertheless, we found that behavioral issues, specifically disinhibition, correlate significantly with baseline caregiver burden in PD patients undergoing DBS surgery. Baseline caregiver burden (as assessed with the CBI) did not change 6 months after DBS despite significantly improved motor function. These findings are important to consider when counseling caregivers and patients about post-surgery expectations regarding caregiver burden. ACKNOWLEDGMENTS We would like to thank Susan Grube and Karen S. Cummings for helping us with data collection. Dr. Soileau has no disclosures. Dr. Persad receives support from NIH grants NS015655-26A1 and AG031951, University of Michigan M-CASTL RFP2010-04. She is also a co-investigator in a clinical trial supported by University Health Network/Michael J Fox Foundation for Parkinson’s Research. Dr. Taylor receives research support from the National Center for Research Resources (NCRR) (grant number UL1RR024986). Dr. Patil receives research support from the National Institutes of Health, the American Parkinson’s Disease Association, the Coulter Foundation, the Foundation for Physical Therapy, the Parkinson’s Disease Foundation, Michigan Institute for Clinical and Health Research, and the University of Michigan Department of Neurosurgery. Dr. Chou receives research support from the NIH (NS44504-08, 5R44NS070438) and the Michael J. Fox Foundation, participates as a site-PI in clinical trials sponsored by the Huntington Study Group (2CARE), receives royalties from UpToDate, receives royalties from Demos Health for his book Deep Brain Stimulation; A New
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Life for People with Parkinson’s, Dystonia, and Essential Tremor, and serves as a consultant for Medtronic and Accordant. CONFLICT OF INTEREST Financial disclosure related to research covered in this article: The authors report no conflicts of interest related to the research covered in this article. REFERENCES [1]
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